key: cord-0879762-u5m1acd9
authors: Patel, Avi; Jenkins, Meg; Rhoden, Kelly; Barnes, Amber N.
title: A Systematic Review of Zoonotic Enteric Parasites Carried by Flies, Cockroaches, and Dung Beetles
date: 2022-01-13
journal: Pathogens
DOI: 10.3390/pathogens11010090
sha: 09d6d85dbb449674e0a7a7f582739958ab8a125a
doc_id: 879762
cord_uid: u5m1acd9

Filth flies, cockroaches, and dung beetles have been close neighbors with humans and animals throughout our joint histories. However, these insects can also serve as vectors for many zoonotic enteric parasites (ZEPs). Zoonoses by ZEPs remain a paramount public health threat due to our close contact with animals, combined with poor water, sanitation, and hygiene access, services, and behaviors in many global regions. Our objective in this systematic review was to determine which ZEPs have been documented in these vectors, to identify risk factors associated with their transmission, and to provide effectual One Health recommendations for curbing their spread. Using PRISMA guidelines, a total of 85 articles published from 1926 to 2021 were reviewed and included in this study. Qualitative analysis revealed that the most common parasites associated with these insects included, but were not limited to: Ascaris spp., Trichuris spp., Entamoeba spp., and Cryptosporidium spp. Additionally, prominent risk factors discovered in the review, such as poor household and community WASH services, unsafe food handling, and exposure to domestic animals and wildlife, significantly increase parasitic transmission and zoonoses. The risk of insect vector transmission in our shared environments makes it critically important to implement a One Health approach in reducing ZEP transmission.

Flies (Diptera), cockroaches (Blattodea), and dung beetles (Coleoptera) share their environment with humans, animals, and other insects. While their presence can be beneficialfor example, through pollination, management of other pests, as a food source, and as an organic disposal system for decaying matter-they can also pose risks to human and animal health. Our close ecological connection to these insects presents the public health risk of disease transmission when one or more vectors are infected or contaminated with pathogenic organisms, such as zoonotic enteric parasites (ZEPs) [1] [2] [3] [4] [5] . ZEPs can be transmitted through direct contact with an insect vector harboring or carrying a parasite, or by accidental fecal-oral ingestion from contaminated food, water, hands, surfaces, and fomites [1] .

Flies, particularly filth flies, are synanthropic and can be found anywhere humans are present, particularly in areas with poor water, sanitation, and hygiene services and practices [6, 7] . Of the 46 species of flies that are associated with unclean environments or conditions of "filth", 21 species are considered "disease-causing flies" or known to be vectors of foodborne pathogens [8] (p. 199). Many species of filth flies are coprophagic, feeding on the fecal waste of animals and humans. While these insects often favor indoor spaces, they frequently move back and forth between contaminated environmental settings and human living spaces. This repeated contact introduces the risk of exposure to enteric diseases of public health concern [1, 8] . Filth flies are drawn to damp, organic matter Table S1 . A formal protocol was not prepared and the review was not registered.

Following PRISMA guidelines, titles were screened first for eligibility based on full and legible citations and journal article titles only [17] . Then, in groups of two reviewers at a time, the titles and abstracts were assessed. Inclusion criteria consisted of titles that were: (a) peer-reviewed journal articles; (b) from any publication year; with (c) primary research documenting the presence of a recognized or probable ZEP in an insect vector, either through natural or experimental infection; and the (d) ZEP has a primarily enteric transmission route. Exclusion criteria comprised: (a) any publication that was not a peerreviewed journal article; (b) titles written in a language other than English without relevant information provided in an English abstract; (c) reviews or models that did not contain primary research; (d) research on vectors other than filth flies, cockroaches, or dung beetles; (e) research on enteric or gastrointestinal parasites that are not considered zoonotic or likely to be zoonotic; or (f) research that included negative results. When an abstract was not available for the first round of screening, the title was included in the next round for full text review. Titles that studied zoonotic enteric parasites not on our initial list of search terms were included after review by the team against the criteria outlined above.

Full text documents were retrieved by the authors and through the assistance of university librarians. Each full text title was reviewed by at least two authors based on the eligibility criteria above and subsequently marked for inclusion or exclusion. The senior author (AB) served as a tie-breaker when needed. If more than one title addressed the same study or data, the more complete publication was retained for inclusion. When the full text of the article was written in a language other than English, the titles were retained if the relevant inclusion criteria were met in an available English abstract. A second round of review was performed on the excluded full-text articles as a quality control measure in order to ensure a comprehensive list of final studies for inclusion.

A qualitative analysis was conducted on the included studies by the reviewers to account for the wide variety of publication styles and research methods presented. From the included studies, data were extracted to determine the publication year, the location of the study site, the source or location of the samples, the vector(s) analyzed, the parasite(s) analyzed, specific prevalence rates, if provided, and the means through which the vector was infected (natural or experimental). Information on risk factors for human or animal transmission outlined in the article was also noted.

The full search resulted in 10,063 accessible titles. We removed 5261 duplicate records, 8 titles that were not legible with the use of automation tools, 311 records with missing citations, and 78 books, book chapters, abstracts, thesis/dissertations, and conference proceedings. At this point, 4406 records remained for the title and abstract screening, and 4099 were excluded using the eligibility criteria outlined above. We attempted to find the full-text versions of 307 titles, but 4 records were not accessible through institutional library channels. A total of 303 articles were read in their entirety, if written in English, or the abstract was reviewed if the full text was not available in English. All titles at this stage were screened against the inclusion/exclusion criteria, and 85 titles were incorporated into the final tally of the study results. Full-text articles were excluded for language (n = 19, missing vector or vector not tested (n = 57), missing zoonotic enteric parasite or not testing for parasite (n = 55), article was a review or did not have primary findings (n = 59), the publication was not a journal article (n = 9), the title was an additional duplicate not removed at the earlier stage (n = 9), or other reasons such as negative results (n = 10). A PRISMA flow diagram of the screening process is available in Figure 1 . publication was not a journal article (n = 9), the title was an additional duplicate not removed at the earlier stage (n = 9), or other reasons such as negative results (n = 10). A PRISMA flow diagram of the screening process is available in Figure 1 . Studies were conducted worldwide, across countries on every continent, except for Antarctica (n = 85; Table 1 ). The most common included the United States (n = 13), Nigeria (n = 7), Ethiopia (n = 5), and Poland (n = 5). More broadly, studies were conducted in the continental regions of North America (n = 13), South America (n = 13), Europe (n = 20), Africa (n = 17), Asia (n = 19), and Australia (n = 2). Publication dates ranged from 1926 through 2021. Several of the studies (n = 11) identified met the inclusion criteria based on an English abstract and were conservatively included in the results. However, the full text could not be analyzed due to language limitations of the authors. Studies were conducted worldwide, across countries on every continent, except for Antarctica (n = 85; Table 1 ). The most common included the United States (n = 13), Nigeria (n = 7), Ethiopia (n = 5), and Poland (n = 5). More broadly, studies were conducted in the continental regions of North America (n = 13), South America (n = 13), Europe (n = 20), Africa (n = 17), Asia (n = 19), and Australia (n = 2). Publication dates ranged from 1926 through 2021. Several of the studies (n = 11) identified met the inclusion criteria based on an English abstract and were conservatively included in the results. However, the full text could not be analyzed due to language limitations of the authors. Table 1 . Characteristics of included studies examining zoonotic enteric parasites of public health concern in flies, cockroaches, and/or dung beetles. 

Most research was conducted on flies (n = 46), followed by cockroaches (n = 33) and dung beetles (n = 8). Two studies investigated two vectors at the same time (Bavay, 1876) , Strongyloides ransomi (Schwartz and Alicata, 1930), Setaria equina (Abildgaard, 1789), Syphacia obvelata (Rudolphi, 1802), Enterobius vermicularis (Linnaeus, 1758), and Oesophagostomus dentatum (Rudolphi, 1803). An acanthocephalan species, Moniliformis (Bremser, 1811) was also named in the study results. The number of studies also varied by insect vector and parasite category, with most of the work investigating protozoa and nematodes in flies and cockroaches (Figure 2 ). While several species of cockroach were investigated among the titles for the presence of zoonotic enteric parasites, the two most common species examined in the included titles in this study were the German cockroach (Blattella germanica; Linnaeus, 1767) and the American cockroach (Periplaneta americana; Linnaeus, 1758). However, additional species were also studied such as Periplaneta brunnea (Burmeister, 1838) , the Cuban burrowing cockroach (Byrsotria fumigata; Guérin-Méneville, 1857), the Madagascar hissing cockroach (Gromphadorhina portentosa; Schaum, 1853), the North American wood roach (Paracoblatta spp.), the oriental cockroach (Blatta orientalis; Linnaeus, 1758), the Turkestan cockroach (Shelfordella lateralis; Walker, 1868), the Australian cockroach (Periplaneta australasiae; Fabricius, 1775), the speckled cockroach (Nauphoeta cinerea; Oliver, 1789), among others.

Within the studies, parasitic pathogens were examined in or on cockroaches. These studies documented the Ascaris spp. Several species of the dung beetle were studied by the included titles to determine if they could harbor, and potentially spread, zoonotic enteric parasites. The dung beetles were from the Scarabaeidae and Geotrupidae families, which primarily feed on fecal or decaying matter. Species came from the Onthophagus genus (e.g., O. fracticornis; Preyssler, 1790), the Bubas genus (e.g., B. bison; Linnaeus, 1767), the Aphodius genus including A. rufus (Moll, 1782) and A. fimetarius (Linnaeus, 1758) , and the Anoplotrupes genus (e.g., A. stercorosus; Scriba, 1791), among others.

Within the titles that examined dung beetles, several parasite pathogens were found to have positive results. These zoonotic enteric parasites found on dung beetles included: Numerous risk factors were mentioned for human and/or animal infection or exposure to zoonotic enteric parasites through insect vectors (Table 2 ). These included poor or inadequate water and sanitation services at home or in the community space (n = 27), having an open defecation site (n = 12) or unmanaged animal waste (n = 16) nearby, insufficient environmental hygiene or the absence of services such as garbage removal (n = 26), seasonal or climatic conditions preferred by the insect vector (n = 14), improper and unsafe food hygiene and storage (n = 23), insect behaviors and feeding practices (n = 29), direct animal contact (n = 22), and ingestion of infected vectors (n = 9). Table 2 . Risk factors for exposure to and/or transmission of zoonotic enteric parasites from flies, cockroaches, or dung beetles, as addressed in the included studies.

Inadequate water and sanitation services or infrastructure at household or community level [10, 18, 19, 21, 23, 33, 37, 38, [40] [41] [42] 44, 52, 54, 59, 61, 64, 70, [72] [73] [74] [75] 78, 81, 82, 89, 100] Open defecation site near human or animal activities [10, 18, 23, 40, 43, 44, 61, 64, 69, 72, 74, 81] Unmanaged animal waste near human or animal activities [10, 26, 28, 31, 36, 40, 43, 44, 46, 50, 60, 66, 74, 81, 94, 100] Poor environmental hygiene, overcrowding, open slaughter, and/or a lack of garbage removal and processing services [35, 38, [40] [41] [42] 44, 47, 52, 54, 55, 58, 64, 67, 70, [72] [73] [74] 76, 78, 81, 82, 84, 88, 89, 91, 100] Seasonality and environmental conditions for insect vector proliferation [18, 28, 29, [38] [39] [40] [41] 62, 69, 71, 82, 90, 91, 97] Unsafe food preparation, storage, sale, and/or service [19] [20] [21] 26, 29, 33, 38, 40, 46, 54, 55, 57, 62, 63, 68, 69, 72, 73, 81, 85, 90, 101] Insect vector feeding behaviors and preferences, movement patterns, and living habitat predilection [19, [29] [30] [31] 34, 35, 39, 43, 46, 49, 52, 54, 55, 57, [59] [60] [61] 64, [71] [72] [73] 76, 79, 85, 86, 88, 90, 97, 101] Animal contact, husbandry, and proximity to living spaces [10, 18, 20, 21, 26, 28, 42, 44, 46, 47, 50, 52, 53, 57, 60, 65, 66, 90, 91, 94, 98, 100] Purposeful or accidental ingestion of contaminated insect vector by animals or humans [25, 30, 34, 56, 66, 72, 75, 95, 96] 

This review highlights the risk of ZEP transmission from insect vectors of interest, including flies, cockroaches, and dung beetles. Flies and cockroaches represent a significant hazard of being exposed to parasites in households and community spaces due to their synanthropic nature [1] . Close cohabitation with humans, especially in the household setting, poses an increased risk of transmission of ZEPs that can be compounded by other factors such as poor sanitation and hygiene. Alternatively, while dung beetles have demonstrated the capability to harbor parasites of public health concern, their preferences for pastures, forest floors, and other natural habitats, coupled with their species-specific dung removal patterns, could actually be of benefit in the removal of zoonotic parasites from the environment [102, 103] .

The included studies in this review were largely centered on filth flies, which feed and reproduce via human and animal fecal waste as well as through organic waste and garbage [6, 7] . Similar to cockroaches, they are drawn to human food items where they may deposit parasitic organisms they have collected via external or internal contamination [1, 7] . The mechanical transmission of ZEPs from these insect vectors in food preparation areas are a danger to health and safety in a variety of settings such as homes, restaurants, and hospitals. Food contamination from these insect vectors may be a neglected global threat to human and animal health.

Many species of zoonotic protozoa were found naturally occurring within the insect vectors examined in the included titles. Additionally, experimental and mixed-methods study designs demonstrated additional vector potential for protozoal transmission. Cockroaches were found to be naturally contaminated with Balantidium spp. [59, 68, 80, 81, 95, 97, 99] . They also harbored the Blastocystis spp. [68, [83] [84] [85] 88, 93, 97, 98, 101] . One title discussed the presence of Blastocystis spp. in cockroaches, but the primary data were presented in a previous study not available in our search results [104, 105] . Both cockroach and fly vectors were found to harbor the Cryptosporidium spp. (cockroach: [47, 59, 68, 89, 95, 97, 99] ; fly: [54, 58, 60, 61, 64, 67, 73, 82, 100] ). However, dung beetles were only infected experimentally [50, 71] . Entamoeba spp. were also found in cockroaches and flies (cockroach: [59, 62, 68, 80, 81, [87] [88] [89] 95, 97, 99] ; fly: [61, 64, 73, 78, 84, 93] ). Contamination with Giardia spp. among flies and cockroaches were common in the included publications (fly: [33, 51, 54, 58, 60, 61, 64, 73, 78, 82, 84, 100] ; cockroach: [80, 88, 89] ). Oocysts from Sarcocystis spp. protozoal parasites were found in cockroaches and flies (cockroach: [34] ; fly: [36] ). Toxoplasma gondii was found in cockroaches, flies, and dung beetles, but only through experimental infection (fly: [22, 24, 26] ; dung beetle: [43] ; cockroach: [28, 31, 34, 46] ).

The insect vectors were found to be naturally contaminated with parasitic worms from the Cestoda class. Flies and cockroaches were found to have naive infection with Hymenolepis spp. (fly: [48, 61, 64, 72, 73, 78] ; cockroach: [76, 89] ). Taenia spp. were reported in flies, cockroaches, and dung beetles (fly: [44, 48, 61, 64, 73, 74, 78] ; cockroach: [62, 68, 76, 80, 95, 97] ; dung beetle: [94] ). Experimental studies showed that flies were also able to harbor Echinococcus spp. [20, 21, 90] . This may have also been true for cockroaches [89] . Moreover, a cockroach was experimentally infected with the D. caninum and Mesocestoides spp. [30] .

The included studies most frequently found parasitic roundworms naturally present in the insect vectors. Ascaris spp. were reported in cockroaches and flies (cockroach: [10, 18, 59, 68, 80, 81, 83, 88, 89, 97] ; fly: [33, [40] [41] [42] 44, 48, 53, 61, 62, 64, [72] [73] [74] 78, 92] ). In addition, flies and cockroaches were found with Capillaria spp. infection (fly: [44, 48, 53] ; cockroach: [10] ). Pinworm, or E. vermicularis, and other Oxyuridae spp. were found naturally occurring in cockroaches and flies (cockroach: [56, 59, 62, 83, 89] ; fly: [53, 72, 78] ). Cockroaches were also experimentally infected with the rat pinworm S. obvelata [30] . Dung beetles were reported to carry Gongylonema spp. [66] . Intestinal hookworms were discovered inside or on the outside of flies and cockroaches (fly: [33, 40, 41, 44, 61, 64, 72, 73] ; cockroach: [10, 76, 89, 97] ). Cockroaches had naïve infections with Physaloptera spp. and Spiruroidea spp. [95] . Strongyloides spp. and Strongyloides-like nematodes spp. were reported in flies and cockroaches (fly: [42, 61, 64, 73] ; cockroach: [59, 68, 80, 89, 97] ). Fly and cockroach vectors were also harboring Toxocara spp. (fly: [42, 44, 48, 53, 77, 84, 91] ; cockroach; [10, 88, 97] ). Natural cockroach infection with Trichinella spp. was reported in the included studies [56] . Additionally, natural Trichostrongylidae spp. infection was reported in flies and cockroaches (fly: [53] ; cockroach: [88] ). Trichuris spp. was also found in fly and cockroach vectors (fly: [33, 40, 41, 44, 48, 53, 61, 64, [72] [73] [74] 78, 91] ; cockroach: [10, 59, 62, 68, 80, 81, 88, 89, 97] ).

Both cockroach and fly vectors were found to be naturally infected with the Acanthocephala spp. (fly: [53] ; cockroach: [32, 95] ). Moreover, cockroaches demonstrated natural infection with Pentastomida spp. [95] .

Within the included studies, several species of enteric parasites that were investigated have a possible, or even probable, zoonotic transmission risk. They include the Cyclospora spp., which were found to be naturally occurring in cockroaches and flies (cockroach: [68, 81, 83, 88, 97, 99] ; fly: [84] ). O. dentatum and T. suis were found in fly samples [92] . Dung beetles were naturally contaminated with T. hydatigena [94] . Additional experimental infection of the insect vectors with Metastrongylus spp., P. turgida, S. equina, S. ransomi, and T. leonina also yielded positive results [30, 65] .

In addition to the pathogenic agents found in the vectors, several of the included studies found non-pathogenic protozoa and flagellate. These organisms often indicate that the vector has had fecal exposure. Entamoeba coli (Grassi, 1879) was found in cockroaches, flies, and dung beetles [23, 33, 61, 62, 64, 68, 73, 78, 84, 88, 93, 97] . Entamoeba hartmanni (Prowazek, 1912) was listed in a cockroach study [93] . Iodamoeba bütschlii (Prowazek, 1912) was also found in flies and cockroaches [68, 78, 88, 93, 97] . Endolimax nana (Wenyon and O'Connor, 1817) was found in dung beetles, cockroaches, and flies [23, 68, 84, 88, 93, 97] . Cockroaches demonstrated naïve infection with the flagellate Chilomastix mesnili (Wenyon, 1910) [68, 88, 97] .

Using the term zoonoses defined as diseases transmitted between humans and vertebrate animals, several pathogens that were found in the insect vectors but do not cause human infection or disease were excluded from the results table [106] . Those included Cystoisopora and Isospora spp., Gregarina spp., Hydatigera (Taenia) taeniaeformis (Batsch, 1786), Hammerschmidtiella diesigni (Hammerschmidt, 1838), Lophomonas battaturm (Stein, 1860), Nyctotherus spp., Pharyngodon spp., and Thelastoma spp. [30, 34, 43, 83, 87, 93, 95, 97, 99, 101] . The inclusion criteria also required that the mode of transmission for the parasite be gastrointestinal, so that it could be considered an enteric parasite. This also excluded Ascaridia galli (Schrank, 1758), Leptomonas spp., Pentatrichomonas spp., and extraintestinal hookworm such as Ancylostoma caninum (Ercolani, 1859) and Uncinaria spp. [30, 42, 83, 91, 93] . Further investigation into the potential role these organisms have in the global parasitic burden of humans and animals is warranted.

The insect vectors analyzed in the included studies originated from natural environments or were reared in laboratory settings. Overall, fly and cockroach insect vectors were collected from farms, pastures, open fields, and nearby livestock housing (i.e., barns) [39, 40, 51, 52, 54, 57, 58, 60, 65, 67, 69, 78, 82, 90, 92, 95, 100] . Fly samples were also drawn from village areas or areas of human habitation such as near kitchens, hospitals, food markets, and schools [27, 33, 38, [40] [41] [42] [43] [44] 54, 60, 61, 64, 69, 72, 73, 77, 78, 100] . Nevertheless, many fly samples were collected near areas with a high risk of environmental contamination such as slaughterhouses/butchers and abattoirs, open defecation sites, and waste disposal or wastewater treatment areas [33, 37, 40, 48, 53, 54, 57, 58, 61, 64, 67, 69, 70, [72] [73] [74] 77, 84, 90] . Some fly specimens were also sampled from areas of public transportation, dog kennels, and from a zoo [33, 36, 53, 91] .

Cockroach specimens were also gathered from villages or household settings or human habitats [10, 18, 32, 37, 47, 55, 56, 59, 62, 63, 68, 72, 76, 80, 81, 83, 85, [87] [88] [89] 97, 99, 101] . Cockroach samples were also collected from a zoo and a pet store [95, 98] . Dung beetles were sampled from wild settings of farms, pastures, forests, and fields [23, 50, 66, 79] . However, one study did examine dung beetles in a village area [94] . Many studies used laboratory insect specimens for their analysis of parasite exposure and vector competence [19] [20] [21] [22] [24] [25] [26] [27] [28] [29] [30] 34, 39, 43, 45, 46, 49, 57, 65, 75, 86, 96] .

The authors of the studies identified water, sanitation, and hygiene-related risk factors that were associated with parasite presence in insect vectors, or were likely to increase the potential for parasite exposure and transmission. Inadequate or unsafe drinking water and sanitation services, infrastructure, and behaviors across individual, household, and community levels may contribute to the spread of ZEPs due to contact with, or food contamination from, flies and cockroaches [10, 18, 19, 21, 23, 33, 37, 38, [40] [41] [42] 44, 52, 54, 59, 61, 64, 70, [72] [73] [74] [75] 78, 81, 82, 89, 100] . Within the larger environment where a household is located, such as within a neighborhood, village, or municipality, potential drivers of ZEP transmission from insect vectors can result from open animal slaughterhouses, garbage and domestic waste piling up without regular removal, overcrowding, and insufficient or unsafe housing structures [35, 38, [40] [41] [42] 44, 47, 52, 54, 55, 58, 64, 67, 70, [72] [73] [74] 76, 78, 81, 82, 84, 88, 89, 91, 100] . In particular, unmanaged, improperly stored, or untreated human waste within our living spaces, such as open defecation sites, may spread zoonotic enteric parasites through insect vectors [10, 18, 23, 40, 43, 44, 61, 64, 69, 72, 74, 81] . Additionally, animal waste near human habitats is also a likely driver of ZEP transmission from insect vectors as they are contaminated by their contact with the human or animal waste for feeding and breeding [10, 26, 28, 31, 36, 40, 43, 44, 46, 50, 60, 66, 74, 81, 94, 100] . Animal-related activities and husbandry in general could serve as a source of contamination for insects and people nearby as well as the animals themselves [10, 18, 20, 21, 26, 28, 42, 44, 46, 47, 50, 52, 53, 57, 60, 65, 66, 90, 91, 94, 98, 100] .

Several of studies mentioned that seasonality and environmental conditions such as rainfall, heat, and humidity could also contribute to the proliferation of the insect vectors and therefore increase the risk of exposure to ZEPs by humans and animals [18, 28, 29, [38] [39] [40] [41] 62, 69, 71, 82, 90, 91, 97] . Moreover, the specific vector feeding, breeding, and habitat preferences coupled with their food predilections could also increase the risk of ZEP transmission [19, [29] [30] [31] 34, 35, 39, 43, 46, 49, 52, 54, 55, 57, [59] [60] [61] 64, [71] [72] [73] 76, 79, 85, 86, 88, 90, 97, 101] . The movements and behaviors of the insects should be considered, especially regarding food contamination. Unsafe food storage, preparation, and sale or service can transmit ZEPs to people and animals after contamination from a vector such as flies or cockroaches [19] [20] [21] 26, 29, 33, 37, 38, 40, 46, 54, 55, 57, 62, 63, 68, 69, 72, 73, 81, 85, 90, 101] . Furthermore, using insects as a food source for humans or animals, whether purposely or accidentally, can also present the risk of ZEP exposure [25, 30, 34, 56, 66, 72, 75, 95, 96] .

One Health studies that simultaneously investigate parasite presence in humans, animals, food, and environmental reservoirs and vectors can demonstrate which groups and exposure pathways may be the biggest threat. For example, a recent publication conducted by a member of this research team found the zoonotic enteric parasites Cryptosporidium spp. and Giardia spp. among human, animals, flies, and drinking water in households in Mongolia [100] . The highest prevalence rate was round in the fly vectors (14.8%). This information, coupled with a household risk factor survey, demonstrated an association between ZEP presence and unimproved drinking water, not having a handwashing site at the home, domestic animal ownership, and rural location [100] . Researchers Dehghani and Kassiri even presented a question regarding the possible role of flies and cockroaches in the ongoing COVID-19 (SARS-CoV-2) pandemic due to their potential for environmental contamination [107] . More holistic research into water, sanitation, and hygiene (WASH) services and behaviors as well as food safety in personal and community spaces in connection with the prevalence of zoonotic enteric parasites in people, animals, and insect vectors who share these environments can shed light on how and where exposures are occurring. Armed with more robust One Health contexts for ZEP transmission routes, public and veterinary health professionals can collaborate with community members on targeted prevention and control efforts.

This review identified studies of ZEPs in cockroaches, filth flies, and dung beetles from all over the world, yet due to the authors' language barriers and lack of qualified translators, only English titles had the full text assessed. English abstracts from several titles illustrated parasite prevalence in vectors of interest and when possible, were included in the final analysis. However, the authors believe that valuable and important work in this subject area is likely to be available in additional languages and found through searching supplemental databases and sources. Furthermore, it is likely that titles of importance were left out of the results due to our search and screening parameters. For example, in one title, the authors spoke of a ZEP in cockroaches but referenced the initial presence data from another source that did not appear in our database results [104, 105] .

The breadth of parasites analyzed in the included studies demonstrate a wide range of species and hosts. In an effort to outline each pathogen, epidemiological details associated with every parasite were omitted. Information on exposure pathways and disease presentation associated with these zoonotic diseases would be helpful for public health professionals, veterinarians, and medical entomologists tasked with using this review for action against ZEP transmission. Similarly, validated information on the current systematic taxa of the pathogens included in the studies could be of further assistance in understanding more about these zoonotic enteric parasites.

One Health research collaboration is needed to build a better global assessment of ZEPs in insect vectors and the risks posed to human, animal, and environmental health. Implementing a joint approach to tackle these complex exposure pathways using experts and stakeholders in the disciplines of public health, epidemiology, veterinary sciences, biology, medical entomology, environmental health, and more can lead to targeted public and veterinary health education messages for the prevention and control of zoonotic enteric parasites.

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Studies on the transmission of helminth ova by cockroaches

Cockroaches as possible transport hosts of Toxoplasma gondii in Costa Rica

Spontaneous parasitism of cockroach (insecta dictyoptera) in Tunis. Their part as an intermediate host of Mastophorus muris (Gmelin 1970) and Moniliformis moniliformis (Bremser 1811). Arch. L'institut Pasteur Tunis

Disease agents carried by flies in Dacca city

Cockroaches as vectors of Sarcocystis muris and of other coccidia in the laboratory

The possible role of the soil fauna in the epizootiology of cysticercosis in cattle. II. Dung beetles-A biotic factor in the transmission of Taenia saginata eggs

Flies as natural transport hosts of Sarcocystis and other coccidia

Transmission of Giardia cysts. I. The role of flies and cockroaches

Laboratory investigations into the role of Musca vicina and Musca domestica in the transmission of parasitic helminth eggs and larvae

The potential role of blowflies in the transmission of taeniid tapeworm eggs

The role of some cyclorrhaphan flies as carriers of human helminths in Malaysia

Human helminth parasite burdens on cyclorrhaphan flies (Diptera) trapped at an aboriginal settlement in Malaysia

Musca domestica as a carrier of intestinal helminths in Calabar

Dung Beetles, Onthophagus spp., as Potential Transport Hosts of Feline Coccidia

A comparison of the role of Musca domestica (Linnaeus) and Chrysomya megacephala (Fabricius) as mechanical vectors of helminthic parasites in a typical slum area of Metropolitan Manila

Influence of host strain and helminth isolate on the first phase of the relationship between rats and Moniliformis moniliformis (Acanthocephala)

Cockroaches as transport hosts of the protozoan Toxoplasma gondii

Childhood Cryptosporidial Diarrhea Associated with Identification of Cryptosporidium sp. in the Cockroach periplaneta Americana

The importance of flies (Diptera-Brachycera) in the dissemination of helminth eggs from sewage treatment plants

House flies (Musca domestica) as transport hosts of Cryptosporidium parvum

The fate of Cryptosporidium parvum oocysts ingested by dung beetles and their possible role in the dissemination of cryptosporidiosis

House fly (Musca domestica) as a transport vector of Giardia lamblia

Mechanical transport and transmission of Cryptosporidium parvum oocysts by wild filth flies

Muscoid dipterans as helminth eggs mechanical vectors at the zoological garden

Detection of Cryptosporidium parvum and Giardia lamblia carried by synanthropic flies by combined fluorescent in situ hybridization and a monoclonal antibody

Cockroaches (Periplaneta americana and Blattella germanica) as potential mechanical disseminators of Entamoeba histolytica

The cockroach as a host for Trichinella and Enterobius vermicularis: Implications for public health

Mechanical transmission of Cryptosporidium parvum oocysts by flies. Wiadomości Parazytol

Cryptosporidium parvum and Giardia lamblia recovered from flies on a cattle farm and in a landfill

Mechanical transmission of pathogenic organisms: The role of cockroaches

Synanthropic flies as vectors of Cryptosporidium and Giardia among livestock and wildlife in a multispecies agricultural complex. Vector-Borne Zoonotic Dis

Non-biting cyclorrhaphan flies (Diptera) as carriers of intestinal human parasites in slum areas of Addis Ababa

Cockroaches as carriers of human intestinal parasites in two localities in Ethiopia

Experimental infection of the cockroach Periplaneta americana with Toxocara canis and the establishment of patent infections in pups

Public health importance of non-biting cyclorrhaphan flies

The house fly (Musca domestica) as a potential vector of metazoan parasites caught in a pig-pen in Germany

A survey of dung beetles infected with larval nematodes with particular note on Copris lunaris beetles as a vector for Gongylonema sp. in Iran

The occurrence of Cryptosporidium spp. in synanthropic flies in urban and rural environments

The majority of cockroaches from the Samutprakarn province of Thailand are carriers of parasitic organisms

Cryptosporidium recovered from Musca domestica, Musca sorbens and mango juice accessed by synanthropic flies in Bahirdar

Unhealthy environment and social aspects associated with intestinal pathogens isolated of dipteral

Effect of dung burial by the dung beetle Bubas bison on numbers and viability of Cryptosporidium oocysts in cattle dung

Cockroaches and flies in mechanical transmission of medical important parasites in Khaldyia Village

Human intestinal parasites in non-biting synanthropic flies in Ogun State

Studies on the potential and public health importance of non-biting synanthropic flies in the mechanical transmission of human enterohelminths

Faecal sludge management with the larvae of the black soldier fly (Hermetia illucens)-From a hygiene aspect

Microbial carriage of cockroaches at a tertiary care hospital in Ghana

Isolation of Toxocara eggs from flies in Northeast Thailand

The housefly Musca domestica L. (Diptera: Muscidae) as a potential paratenic host in the city of Bom Jesus-Piauí

Longevity and viability of Taenia solium eggs in the digestive system of the beetle Ammophorus rubripes

Isolation of intestinal parasites of public health importance from cockroaches (Blattella germanica) in Jimma Town, Southwestern Ethiopia

Comparative analysis of pathogenic organisms in cockroaches from different community settings in Edo State

Genotyping and subtyping Cryptosporidium parvum and Giardia duodenalis carried by flies on dairy farms in Henan, China. Parasites Vectors

Isolation of intestinal parasites from American cockroach (Periplaneta americana) in Coro, Falcon state

Bacterial and Parasite Agents in Adult Housefly Musca domestica Collected in El Peñón, Sucre State

Short Communication Current status of Blastocystis in cockroaches

Experimental transmission of Toxocara canis from Blattella germanica and Periplaneta americana cockroaches to a paratenic host

The prevalence of protozoa in the gut of German cockroaches (Blattella germanica) with special reference to Lophomonas blattarum

First investigation on vectorial potential of Blattella germanica in Turkey

Domiciliary cockroaches as carriers of human intestinal parasites in Lagos Metropolis, Southwest Nigeria: Implications for public health

Experimental and field investigation of non-biting flies as potential mechanical vectors of Echinococcus granulosus eggs

Contamination of animal-keeping premises with eggs of parasitic worms

Enteroparasitary contamination of flies captured in the Palavecino municipality, Lara state

Cysticercosis Working Group in Peru. Molecular detection of taeniid eggs in beetles collected in an area endemic for Taenia solium

A parasitological evaluation of edible insects and their role in the transmission of parasitic diseases to humans and animals

Risk evaluation of passive transmission of animal parasites by feeding of black soldier fly (Hermetia illucens) larvae and prepupae

Prevalence of parasitic contamination of cockroaches collected from fresh markets in Chachoengsao province

Cockroach as a Vector of Blastocystis sp. is Risk for Golden Monkeys in Zoo

Protozoan cysts in faecal pellets of German cockroaches (Blattella germanica), with particular emphasis on Lophomonas blattarum

Zoonotic enteric parasites in Mongolian people, animals, and the environment: Using One Health to address shared pathogens

First report of Lophomonoas spp. in German Cockroaches (Blatella germanica) Trapped in Hospitals, Northern Iran

Dung beetles reduce livestock gastrointestinal parasite availability on pasture

Dung beetles as biological control agents for gastrointestinal parasites of livestock

Ultrastructural and phylogenetic studies on Blastocystis isolates from cockroaches

Isolation of Blastocystis from the cockroach (Dictyoptera: Blattidae)

A brief review on the possible role of houseflies and cockroaches in the mechanical transmission of coronavirus disease 2019 (COVID-19)